Rehabilitative exercise in a rat model of doxorubicin cardiotoxicity

Experimental Biology and Medicine

Volumn 237, Issue 12, 2012, Pages 1483-1492

  Hydock, David S ^a   Lien, Chia Ying ^b   Jensen, Brock T ^c   Parry, Traci L ^a   Schneider, Carole M ^a   Hayward, Reid ^a  

^a UNIVERSITY OF NORTHERN COLORADO   (United States)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c SLIPPERY ROCK UNIVERSITY   (United States)

Author keywords

Adriamycin; Anthracycline; Heart failure; Physical activity

Indexed keywords

DOXORUBICIN; MYOSIN HEAVY CHAIN; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD FLOW VELOCITY; CARDIOTOXICITY; CONTROLLED STUDY; DENSITOMETRY; ECHOCARDIOGRAPHY; EX VIVO STUDY; FEMALE; HEART FUNCTION; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART SIZE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; RAT; TREADMILL;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CARDIOTOXINS; DISEASE MODELS, ANIMAL; DOXORUBICIN; ECHOCARDIOGRAPHY, THREE-DIMENSIONAL; EXERCISE THERAPY; FEMALE; HEART DISEASES; MYOCARDIUM; MYOSIN HEAVY CHAINS; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84873024790     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1258/ebm.2012.012137     Document Type: Article

References (52)

1. Bernstein D, Fajardo G, Zhao M, Urashima T, Powers J, Berry G, Kobilka BK. Differential cardioprotective/cardiotoxic effects mediated by beta-adrenergic receptor subtypes. Am J Physiol Heart Circ Physiol 2005;289:H2441-2449
2. Chicco AJ, Schneider CM, Hayward R. Exercise training attenuates acute doxorubicin-induced cardiac dysfunction. J Cardiovasc Pharmacol 2006;47:182-9
3. Hydock DS, Lien CY, Schneider CM, Hayward R. Exercise preconditioning protects against doxorubicin-induced cardiac dysfunction. Med Sci Sports Exerc 2008;40:808-17
4. Arnolda L, McGrath B, Cocks M, Sumithran E, Johnston C. Adriamycin cardiomyopathy in the rabbit: an animal model of low output cardiac failure with activation of vasoconstrictor mechanisms. Cardiovasc Res 1985;19:378-82
5. Hayward R, Hydock DS. Doxorubicin cardiotoxicity in the rat: an in vivo characterization. J Am Assoc Lab Anim Sci 2007;46:20-32
6. Abu-Khalaf MM, Juneja V, Chung GG, DiGiovanna MP, Sipples R, McGurk M, Zelterman D, Haffty B, Reiss M, Wackers FJ, Lee FA, Burtness BA. Long-term assessment of cardiac function after dose-dense and-intense sequential doxorubicin (A), paclitaxel (T), and cyclophosphamide (C) as adjuvant therapy for high risk breast cancer. Breast Cancer Res Treat 2007;104:341-9
7. Pein F, Sakiroglu O, Dahan M, Lebidois J, Merlet P, Shamsaldin A, Villain E, de Vathaire F, Sidi D, Hartmann O. Cardiac abnormalities 15 years and more after adriamycin therapy in 229 childhood survivors of a solid tumour at the Institut Gustave Roussy. Br J Cancer 2004;91:37-44
8. de Beer EL, Bottone AE, van Der Velden J, Voest EE. Doxorubicin impairs crossbridge turnover kinetics in skinned cardiac trabeculae after acute and chronic treatment. Mol Pharmacol 2000;57:1152-7
9. Hydock DS, Lien CY, Jensen BJ, Parry TL, Malcolm WT, Schneider CM, Hayward R. Concurrent wheel running and weekly doxorubicin treatment in the rat: effects on cardiac function. Med Sci Sports Exerc 2010;42:3
10. Hydock DS, Lien CY, Jensen BT, Schneider CM, Hayward R. Exercise preconditioning provides long-term protection against early chronic doxorubicin cardiotoxicity. Integr Cancer Ther 2011;10:47-57
11. Liu TC, Ismail S, Brennan O, Hastings C, Duffy GP. Encapsulation of cardiac stem cells in superoxide dismutase-loaded alginate prevents doxorubicin-mediated toxicity. J Tissue Eng Regen Med 2011; Epub ahead of print: doi:10.1002/term.523
12. Xu X, Chen K, Kobayashi S, Timm D, Liang Q. Resveratrol Attenuates doxorubicin-induced cardiomyocyte death via inhibition of S6k1-mediated autophagy. J Pharmacol Exp Ther 2012;341:183-95
13. Xiao J, Sun GB, Sun B, Wu Y, He L, Wang X, Chen RC, Cao L, Ren XY, Sun XB. Kaempferol protects against doxorubicin-induced cardiotoxicity in vivo and in vitro. Toxicology 2012;292:53-62
14. Wang X, Wang Q, Guo W, Zhu YZ. Hydrogen sulfide attenuates cardiac dysfunction in a rat model of heart failure: a mechanism through cardiac mitochondrial protection. Biosci Rep 2011;31:87-98
15. Takemura G, Fujiwara H. Doxorubicin-induced cardiomyopathy from the cardiotoxic mechanisms to management. Prog Cardiovasc Dis 2007;49:330-52
16. Ascensao A, Magalhaes J, Soares J, Ferreira R, Neuparth M, Marques F, Oliveira J, Duarte J. Endurance training attenuates doxorubicin-induced cardiac oxidative damage in mice. Int J Cardiol 2005;100:451-60
17. Wonders KY, Hydock DS, Schneider CM, Hayward R. Acute exercise protects against doxorubicin cardiotoxicity. Integr Cancer Ther 2008;7:147-54
18. Fairclough DL, Fetting JH, Cella D, Wonson W, Moinpour CM. Quality of life and quality adjusted survival for breast cancer patients receiving adjuvant therapy. Eastern Cooperative Oncology Group (ECOG). Qual Life Res 1999;8:723-31
19. Liu J, Tu D, Dancey J, Reyno L, Pritchard KI, Pater J, Seymour LK. Quality of life analyses in a clinical trial of DPPE (tesmilifene) plus doxorubicin versus doxorubicin in patients with advanced or metastatic breast cancer: NCIC CTG Trial MA.19. Breast Cancer Res Treat 2006;100:263-71
20. Schneider CM, Hsieh CC, Sprod LK, Carter SD, Hayward R. Exercise training manages cardiopulmonary function and fatigue during and following cancer treatment in male cancer survivors. Integr Cancer Ther 2007;6:235-41
21. Schneider CM, Hsieh CC, Sprod LK, Carter SD, Hayward R. Effects of supervised exercise training on cardiopulmonary function and fatigue in breast cancer survivors during and after treatment. Cancer 2007;110:918-25
22. Burnham TR, Wilcox A. Effects of exercise on physiological and psychological variables in cancer survivors. Med Sci Sports Exerc 2002;34:1863-7
23. Chicco AJ, Hydock DS, Schneider CM, Hayward R. Low-intensity exercise training during doxorubicin treatment protects against cardiotoxicity. J Appl Physiol 2006;100:519-27
24. Hydock DS, Wonders KY, Schneider CM, Hayward R. Voluntary wheel running in rats receiving doxorubicin: effects on running activity and cardiac myosin heavy chain. Anticancer Res 2009;29:4401-7
25. Fornier MN, Seidman AD, Theodoulou M, Moynahan ME, Currie V, Moasser M, Sklarin N, Gilewski T, D'Andrea G, Salvaggio R, Panageas KS, Norton L, Hudis C. Doxorubicin followed by sequential paclitaxel and cyclophosphamide versus concurrent paclitaxel and cyclophosphamide: 5-year results of a phase II randomized trial of adjuvant dose-dense chemotherapy for women with node-positive breast carcinoma. Clin Cancer Res 2001;7:3934-41
26. Bonadonna G, Zambetti M, Valagussa P. Sequential or alternating doxorubicin and CMF regimens in breast cancer with more than three positive nodes. Ten-year results. JAMA 1995;273:542-7
27. Christie J, Sheldahl LM, Tristani FE, Sagar KB, Ptacin MJ, Wann S. Determination of stroke volume and cardiac output during exercise: comparison of two-dimensional and Doppler echocardiography, Fick oximetry, and thermodilution. Circulation 1987;76:539-47
28. Hydock DS, Lien CY, Schneider CM, Hayward R. Effects of voluntary wheel running on cardiac function and myosin heavy chain in chemically gonadectomized rats. Am J Physiol Heart Circ Physiol 2007;293:H3254-3264
29. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-54
30. Ascensao A, Ferreira R, Oliveira PJ, Magalhaes J. Effects of endurance training and acute Doxorubicin treatment on rat heart mitochondrial alterations induced by in vitro anoxia-reoxygenation. Cardiovasc Toxicol 2006;6:159-72
31. Ascensao A, Magalhaes J, Soares JM, Ferreira R, Neuparth MJ, Marques F, Oliveira PJ, Duarte JA. Moderate endurance training prevents doxorubicin-induced in vivo mitochondriopathy and reduces the development of cardiac apoptosis. Am J Physiol Heart Circ Physiol 2005;289:H722-731
32. Hydock DS, Lien CY, Jensen BT, Schneider CM, Hayward R. Exercise preconditioning provides long-term protection against early chronic doxorubicin cardiotoxicity. Integr Cancer Ther 2011;10:47-57
33. Chicco AJ, Schneider CM, Hayward R. Voluntary exercise protects against acute doxorubicin cardiotoxicity in the isolated perfused rat heart. Am J Physiol Regul Integr Comp Physiol 2005;289:R424-31
34. Wonders KY, Hydock DS, Greufe S, Schneider CM, Hayward R. Endurance exercise training preserves cardiac function in rats receiving doxorubicin and the HER-2 inhibitor GW2974. Cancer Chemother Pharmacol 2009;64:1105-13
35. Ascensao A, Oliveira PJ, Magalhaes J. Exercise as a beneficial adjunct therapy during Doxorubicin treatment-Role of mitochondria in cardioprotection. Int J Cardiol 2012;156:4-10
36. Nousiainen T, Jantunen E, Vanninen E, Hartikainen J. Early decline in left ventricular ejection fraction predicts doxorubicin cardiotoxicity in lymphoma patients. Br J Cancer 2002;86:1697-700
37. Huang C, Zhang X, Ramil JM, Rikka S, Kim L, Lee Y, Gude NA, Thistlethwaite PA, Sussman MA, Gottlieb RA, Gustafsson AB. Juvenile exposure to anthracyclines impairs cardiac progenitor cell function and vascularization resulting in greater susceptibility to stress-induced myocardial injury in adult mice. Circulation 2010;121:675-83
38. Simunek T, Sterba M, Popelova O, Adamcova M, Hrdina R, Gersl V. Anthracycline-induced cardiotoxicity: overview of studies examining the roles of oxidative stress and free cellular iron. Pharmacol Rep 2009;61:154-71
39. Wang Y, Wisloff U, Kemi OJ. Animal models in the study of exercise-induced cardiac hypertrophy. Physiol Res 2010;59:633-44
40. Natali AJ, Turner DL, Harrison SM, White E. Regional effects of voluntary exercise on cell size and contraction-frequency responses in rat cardiac myocytes. J Exp Biol 2001;204:1191-9
41. Starnes JW, Taylor RP, Ciccolo JT. Habitual low-intensity exercise does not protect against myocardial dysfunction after ischemia in rats. Eur J Cardiovasc Prev Rehabil 2005;12:169-74
42. Hydock DS, Lien CY, Jensen BJ, Parry TL, Schneider CM, Hayward R. Cardioprotective effects of voluntary wheel running during and following doxorubicin treatment. Med Sci Sports Exerc 2009;41:118
43. Herron TJ, McDonald KS. Small amounts of alpha-myosin heavy chain isoform expression significantly increase power output of rat cardiac myocyte fragments. Circ Res 2002;90:1150-2
44. Korte FS, Herron TJ, Rovetto MJ, McDonald KS. Power output is linearly related to MyHC content in rat skinned myocytes and isolated working hearts. Am J Physiol Heart Circ Physiol 2005;289:H801-812
45. Jin H, Yang R, Li W, Lu H, Ryan AM, Ogasawara AK, Van Peborgh J, Paoni NF. Effects of exercise training on cardiac function, gene expression, and apoptosis in rats. Am J Physiol Heart Circ Physiol 2000;279:H2994-3002
46. Olson RD, Gambliel HA, Vestal RE, Shadle SE, Charlier HA Jr, Cusack BJ. Doxorubicin cardiac dysfunction: effects on calcium regulatory proteins, sarcoplasmic reticulum, and triiodothyronine. Cardiovasc Toxicol 2005;5:269-83
47. Park KH, Kim SY, Gul R, Kim BJ, Jang KY, Chung HT, Sohn DH. Fatty acids ameliorate doxorubicin-induced intracellular ca2+ increase and apoptosis in rat cardiomyocytes. Biol Pharm Bull 2008;31:809-15
48. Kim SY, Kim SJ, Kim BJ, Rah SY, Chung SM, Im MJ, Kim UH. Doxorubicin-induced reactive oxygen species generation and intracellular Ca2+ increase are reciprocally modulated in rat cardiomyocytes. Exp Mol Med 2006;38:535-45
49. Kemi OJ, Ceci M, Condorelli G, Smith GL, Wisloff U. Myocardial sarcoplasmic reticulum Ca2+ ATPase function is increased by aerobic interval training. Eur J Cardiovasc Prev Rehabil 2008;15:145-8
50. Lee Y, Min K, Talbert EE, Kavazis AN, Smuder AJ, Willis WT, Powers SK. Exercise protects cardiac mitochondria against ischemia-reperfusion injury. Med Sci Sports Exerc 2012;44:397-405
51. French JP, Hamilton KL, Quindry JC, Lee Y, Upchurch PA, Powers SK. Exercise-induced protection against myocardial apoptosis and necrosis: MnSOD, calcium-handling proteins, and calpain. Faseb J 2008;22:2862-71
52. Yoshida M, Shiojima I, Ikeda H, Komuro I. Chronic doxorubicin cardiotoxicity is mediated by oxidative DNA damage-ATM-p53-apoptosis pathway and attenuated by pitavastatin through the inhibition of Rac1 activity. J Mol Cell Cardiol 2009;47:698-705